Interindividual differences in memory system local field potential activity predict behavioral strategy on a dual‐solution T‐maze

Abstract

Individuals can use diverse behavioral strategies to navigate their environment including hippocampal-dependent place strategies reliant upon cognitive maps and striatal-dependent response strategies reliant upon egocentric body turns. The existence of multiple memory systems appears to facilitate successful navigation across a wide range of environmental and physiological conditions. The mechanisms by which these systems interact to ultimately generate a unitary behavioral response, however, remain unclear. We trained 20 male, Sprague-Dawley rats on a dual-solution T-maze while simultaneously recording local field potentials that were targeted to the dorsolateral striatum and dorsal hippocampus. Eight rats spontaneously exhibited a place strategy while the remaining 12 rats exhibited a response strategy. Interindividual differences in behavioral strategy were associated with distinct patterns of LFP activity between the dorsolateral striatum and dorsal hippocampus. Specifically, striatalhippocampal theta activity was in-phase in response rats and out-of-phase in place rats and response rats exhibited elevated striatal-hippocampal coherence across a wide range of frequency bands. These contrasting striatal-hippocampal activity regimes were (a) present during both maze-learning and a 30 min premaze habituation period and (b) could be used to train support vector machines to reliably predict behavioral strategy. Distinct patterns of neuronal activity across multiple memory systems, therefore, appear to bias behavioral strategy selection and thereby contribute to interindividual differences in behavior.

Understanding Differences in Wayfinding Strategies

“…Other tasks, such as the radial arm maze, have also revealed differences in place and response learning, particularly with regard to distal landmarks (Iaria et al, 2003). Moreover, similar individual differences in spontaneous navigation strategies have been found in animals, and are associated with distinct patterns of neural activity between the striatum and hippocampus (Goldenberg, Lentzou, Ackert-Smith, Knowlton, & Dash, 2020). Boone, Gong, and Hegarty (2018) found sex differences in navigation strategies, such that men were more likely to use place-based (shortcut) strategies in the DSP, while women more often used the response-based strategy of following the learned route, as illustrated in Fig.…”

Loss of GABA co-transmission from cholinergic neurons impairs behaviors related to hippocampal, striatal, and medial prefrontal cortex functions

“…During striatal learning, the dorsolateral striatum undergoes changes in neuron firing, cell signaling, as well as epigenetic modifications (Aosaki et al, 1994b ; Jog et al, 1999 ; Kheirbek et al, 2009 ; Zhang and Cragg, 2017 ; Malvaez et al, 2018 ). These changes likely enable the synchronization between the striatum and hippocampus leading to increased mPFC activity (Doeller and Burgess, 2008 ; Doeller et al, 2008 ; Rich and Shapiro, 2009 ; Goldenberg et al, 2020 ). Given the importance of ACh neurons in striatal learning and function, loss of GABA co-transmission may disrupt corticostriatal inhibition, striatal output, strengthen striatal extinction mechanisms, or reduce synchrony between the hippocampus, the mPFC, and striatum (Aosaki et al, 1994a ; Chang and Gold, 2003 ; Lozovaya et al, 2018 ; Goldenberg et al, 2020 ; Fleming et al, 2022 ).…”

“…These changes likely enable the synchronization between the striatum and hippocampus leading to increased mPFC activity (Doeller and Burgess, 2008 ; Doeller et al, 2008 ; Rich and Shapiro, 2009 ; Goldenberg et al, 2020 ). Given the importance of ACh neurons in striatal learning and function, loss of GABA co-transmission may disrupt corticostriatal inhibition, striatal output, strengthen striatal extinction mechanisms, or reduce synchrony between the hippocampus, the mPFC, and striatum (Aosaki et al, 1994a ; Chang and Gold, 2003 ; Lozovaya et al, 2018 ; Goldenberg et al, 2020 ; Fleming et al, 2022 ). We, therefore, conclude that GABA co-transmission is a minor regulator of response learning with possible relevance to altered learning strategies in addiction, autism spectrum disorders, schizophrenia, or PD (Graybiel and Rauch, 2000 ; Redgrave et al, 2010 ).…”

Loss of GABA co-transmission from cholinergic neurons impairs behaviors related to hippocampal, striatal, and medial prefrontal cortex functions

“…During striatal learning, the dorsolateral striatum undergoes changes in neuron firing, cell signaling, as well as epigenetic modifications (Aosaki et al (1994b), Zhang and Cragg (2017), Jog et al (1999), Kheirbek et al (2009), Malvaez et al (2018)). These changes likely enable the synchronization between striatum and hippocampus leading to increased mPFC activity (Doeller and Burgess (2008), Doeller et al (2008), Goldenberg et al (2020)). Given the importance of ACh neurons in striatal learning and function, loss of GABA co-transmission may disrupt corticostriatal inhibition, striatal output, strengthen striatal extinction mechanisms, or reduce synchrony between the hippocampus, the mPFC, and striatum (Aosaki et al (1994a), Chang and Gold (2003), Lozovaya et al (2018), Goldenberg et al (2020), Fleming et al (2022)).…”

“…These changes likely enable the synchronization between striatum and hippocampus leading to increased mPFC activity (Doeller and Burgess (2008), Doeller et al (2008), Goldenberg et al (2020)). Given the importance of ACh neurons in striatal learning and function, loss of GABA co-transmission may disrupt corticostriatal inhibition, striatal output, strengthen striatal extinction mechanisms, or reduce synchrony between the hippocampus, the mPFC, and striatum (Aosaki et al (1994a), Chang and Gold (2003), Lozovaya et al (2018), Goldenberg et al (2020), Fleming et al (2022)). We, therefore, conclude that GABA co-transmission is a minor regulator of response learning with possible relevance to altered learning strategies in addiction, autism spectrum disorders, schizophrenia, or PD (Graybiel and Rauch (2000), Redgrave et al (2010)).…”